Transactions on Science and Technology, 3(2-2), 374 - 381, 2016
ISSN: 2289-8786
Gene Expression in the Biosynthesis of Paralytic Shellfish Poisoning (PSP) Toxins in Dinoflagellates: A Mini Review

Adrianne Suk Wai Leong, Ann Anton, Kenneth Francis Rodrigues, Grace Joy Wei Lie Chin
ABSTRACT
Some dinoflagellates are known to synthesize saxitoxin (STX), a potent neurotoxin that causes severe paralytic shellfish poisoning (PSP). In addition, several freshwater species of cyanobacteria also synthesize the same toxin with the same biosynthetic pathway and genes responsible. This review focuses on the gene expression involved in the biosynthesis pathway of PSP toxins in dinoflagellates. The expression of the PSP biosynthetic genes have been identified in certain cyanobacteria and the dinoflagellate Alexandrium sp. with eight genes involved viz. sxtA, sxtB, sxtD, sxtG, sxtH/T, sxtI, sxtS and sxtU. sxtA, a unique starting gene, and sxtG, the second “core” gene appearing in the biosynthesis of PSP toxins are found in both cyanobacteria and Alexandrium sp. Three theories have been proposed to explain the origin of PSP toxin in dinoflagellates: I) the genes are produced by bacteria associated with the dinoflagellates, II) independent evolution III) horizontal gene transfer between cyanobacteria and dinoflagellates. Useful information regarding the expression and function of genes involved in the STX biosynthesis pathway provides an understanding of toxin production and possible mitigation and public health management of STX poisoning.

Keywords:
Paralytic shellfish toxins; harmful algal blooms; dinoflagellates; transcriptome genes; saxitoxin biosynthesis

Full Text PDF

© Transactions on Science and Technology 2016

References

[1]    Chang, F., Anderson, D. M., Kulis, D. M. & Till, D. G. (1997). Toxin production of Alexandrium minutum (Dinophyceae) from the Bay of Plenty, New Zealand. Toxicon, 35, 393-409.

[2]    Chen, L., Zhang, H., Finiguerra, M., Bobkov, Y., Bouchard, C., Avery, D. E., Anderson, P. A. V., Lin, S. & Dam, H. G. (2015). A novel mutation from gene splicing of a voltage-gated sodium channel in a marine copepod and its potential effect on channel function. Journal of Experimental Marine Biology and Ecology, 469, 131-142.

[3]    Doucette, G. J. (1995). Interactions between bacteria and harmful algae: a review. Natural Toxins, 3, 65-74.

[4]    Faber, S. (2012). Saxitoxin and the induction of paralytic shellfish poisoning. Journal of Young Investigators, 23, 1-7.

[5]    Gallacher, S., Flynn, K. J., Franco, J. M., Brueggemann, E. E. & Hines, H. B. (1997). Evidence for production of paralytic shellfish toxins by bacteria associated with Alexandrium spp. (Dinophyta) in culture. Applied and Environmental Microbiology, 63(1), 239-245.

[6]    Hackett, J. D., Wisecaver, J. H., Brosnahan, M. L., Kulis, D. M., Anderson, D. M., Bhattacharya, D., Plumley, F. G. & Erdner, D. L. (2013). Evolution of saxitoxin synthesis in cyanobacteria and dinoflagellates. Molecular Biology Evolution, 30(1), 70-78.

[7]    Hansen, G., Daugbjerg, N. & Franco, J. M. (2003). Morphology, toxin composition and LSU rDNA phylogeny of Alexandrium minutum (Dinophyceae) from Denmark, with some morphological observations on other European strains. Harmful Algae, 2, 317-335.

[8]    Hii, K. S., Lim, P. T., Kon, N. F., Takata, Y., Usup, G. & Leaw, C. P. (2016). Physiological andtranscriptional responses to inorganic nutrition in a tropical Pacific strain of Alexandrium minutum: Implications for the saxitoxin genes and toxin production. Harmful Algae, 56, 9-21.

[9]    Hold, G. L., Smith, E. A., Birkbeck, T. H. & Gallacher, S. (2001). Comparison of paralytic shellfish toxin (PST) production by the dinoflagellates Alexandrium lusitanicum NEPCC 253 and Alexandrium tamarense NEPCC 407 in the presence and absence of bacteria. FEMS Microbiology Ecology, 36, 223-234.

[10]  Humpage, A. R., Rositano, J., Bretag, A., Brown, R. Baker, P., Nicholson, B. C. & Steffensen, D. A. (1994). Paralytic shellfish poisons from Australian blue-green algal (cyanobacteria) blooms. Australian Journal of Marine and Freshwater Research, 45, 761-771.

[11]  John, U., Litaker, R. W., Montresor, M., Murray, S., Brosnahan, M. L. & Anderson, D. M. (2014) Formal revision of the Alexandrium tamarense species complex (Dinophyceae) taxonomy: the introduction of five species with emphasis on molecular-based (rDNA) classification. Protist, 165(6), 779-804.

[12]  Kellmann, R., Mihali, T. K., Jeon, Y. J., Pickford, R., Pomati, F. & Neilan, B. A. (2008). Biosynthetic intermediate analysis and functional homology reveal a saxitoxin gene cluster in cyanobacteria. Applied Environmental Microbiology, 74(13), 4044-4053.

[13]  Lagos, N., Onodera, H., Zagatto, P. A., Andrinolo, D., Azevedo, S. M. F. Q. & Oshima, Y. (1999). The first evidence of paralytic shellfish toxins in the freshwater cyanobacterium Cylindrospermopsis raciborskii, isolated from Brazil. Toxicon, 37, 1359-1373.

[14]  Lin, S. J. (2011). Genomic understanding of dinoflagellates. Research in Microbiology, 162(6): 551-569.

[15]  Morozova, O. & Marra, M. A. (2008). Applications of next-generation sequencing technologies in functional genomics. Genomics, 92, 255-264.

[16]  Murray, S. A., Wiese, M., Stuken, A., Brett, S., Kellmann, R., Hallegraeff, G. & Neilan, B. A. (2011). SxtA-based quantitative molecular assay to identify saxitoxin-producing harmful algal blooms in marine waters. Applied and Environmental Microbiology, 77(19), 7050-7057

[17]  Onodera, H., Satake, M., Oshima, Y., Yasumoto, T. & Carmichael, W.W. (1997). New saxitoxin analogues from the freshwater filamentous cyanobacterium Lyngbya wollei. Natural Toxins, 5, 146-151.

[18]  Organization for the prohibitation of chemical weapons (OPCW) (2008). Toxins (https://www.opcw.org/protection/types-of-chemical-agent/toxins/). Accesssed on 8 August 2016.

[19]  Orr, R. J. S., Stuken, A., Murray, S. A. & Jakobsen, K. S. (2013). Evolutionary acquisition and loss of saxitoxin biosynthesis in dinoflagellates: The second “core” gene—sxtG. Applied and Environmental Microbiology, 79(7), 2128-2136.

[20]  Oshima, Y., Blackburn, S. I. & Hallegraeff, G. M. (1993). Comparative study on paralytic shellfish toxin profiles of the dinoflagellate Gymnodinium catenatum from three different countries. Marine Biology, 116, 471-476.

[21]  Palacios, L., Reguera, B., Franco, J. & Marin, I. (2006). Phylogenetic diversity of bacteria associated with toxic and non-toxic strains of Alexandrium minutum. African Journal of Marine Science, 28(2), 409-414.

[22]  Perini, F., Galluzzi, L., Dell’Aversano, C., Dello Iacovo, E., Tartaglione, L., Ricci, F., Forino, M., Ciminiello, P. & Penna, A. (2014). sxtA and sxtG gene expression and toxin production in the Mediterranean Alexandrium minutum (Dinophyceae). Marine Drugs, 12, 5258-5276.

[23]  Shimizu, Y. (1993). Microalgal metabolites. Chemical Reviews, 93, 1685-1698.

[24]  Shimizu, Y. (1996). Microalgal metabolites: a new perspective. Annual Review Microbiology, 50, 431-465.

[25]  Silva, S. E. (1990). Intracellular bacteria: the origin of dinoflagellate toxicity. Journal of Environmental Pathology Toxicology and Oncology, 10,124-128.

[26]  Stuken, A., Orr, R. J. S., Kellmann, R., Murray, S. A., Neilan, B. A. & Jakobsen, K. S. (2011). Discovery of nuclear-encoded genes for the neurotoxin saxitoxin in dinoflagellates. PLoS One, 6(5).

[27]  Usup, G., Kulis, D. M. & Anderson, D. M. (1994). Growth and toxin production of the toxic dinoflagellate Pyrodinium bahamense var. compressum in laboratory cultures. Natural Toxins, 2, 254-262.

[28]  Usup, G., Cheah, M. Y., Ng, B. K., Leaw, C. P. & Ahmad, A. (2006). Toxin profile and relative toxicity of three paralytic shellfish poisoning toxin-producing dinoflagellates from Malaysia. Malaysian Applied Biology, 35(2), 41-45.

[29]  Usup, G., Ahmad, A., Matsuoka, K., Lim, P. T. & Leaw, C. P. (2012). Biology, ecology, and bloom dynamics of the toxic marine dinoflagellate Pyrodinium bahamense. Harmful Algae, 14, 301-312.

[30]  Wang, D. Z. (2008). Neurotoxins from marine dinoflagellates: a brief review. Marine Drugs, 6, 349-371.

[31]  Wang, L., Zhuang, Y., Zhang, H., Lin, X. & Lin, S. (2014). DNA barcoding species in Alexandrium tamarense complex using ITS and proposing designation of five species. Harmful Algae, 31, 100-113.

[32]         Wiese, M., D’Agostino, P. M., Mihali, T. K., Moffitt, M. C. & Neilan, B. A. (2010). Neurotoxic alkaloids: saxitoxin and its analogs. Marine Drugs 8, 2185-2211.